Natural selection and repeated patterns of molecular evolution following allopatric divergence
- North Carolina State University, United States
- University of Florida, United States
- Beijing Genomics Institute, China
- Chinese Academy of Sciences, China
- Zhejiang University, China
Abstract
Although geographic isolation is a leading driver of speciation, the tempo and pattern of divergence at the genomic level remain unclear. We examine genome-wide divergence of putatively single-copy orthologous genes (POGs) in 20 allopatric species/variety pairs from diverse angiosperm clades, with 16 pairs reflecting the classic eastern Asia-eastern North America floristic disjunction. In each pair, >90% of POGs are under purifying selection, and <10% are under positive selection. A set of POGs are under strong positive selection, 14 of which are shared by 10-15 pairs, and one shared by all pairs; 15 POGs are annotated to biological processes responding to various stimuli. The relative abundance of POGs under different selective forces exhibits a repeated pattern among pairs despite an ~10-million-year difference in divergence time. Species divergence times are positively correlated with abundance of POGs under moderate purifying selection, but negatively correlated with abundance of POGs under strong purifying selection.
Data availability
Sequences of ortologous gene families and pairs of POGs sequences used for calculation of Ka and Ks have been submitted to Dryad (https://datadryad.org//). Raw transcriptome data have been submitted to NCBI SRA database with Bioproject number PRJNA508825 and Biosample number from SAMN10534244 to SAMN10534283 (Supplementary File 11).
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Natural selection and repeated patterns of molecular evolution following allopatric divergenceBioproject number PRJNA508825 and Biosample number from SAMN10534244 to SAMN10534283.
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Data from: Natural selection and repeated genome-wide patterns of molecular evolution following allopatric divergenceDryad Digital Repository, 10.5061/dryad.f1f0q44.
Article and author information
Author details
Funding
National Science Foundation (DEB-442161)
- Yibo Dong
- Wenbin Zhou
- Jenny Xiang
National Science Foundation (DEB-442280)
- Shichao Chen
- Pamela S Soltis
- Douglas E Soltis
National Science Foundation of China (IOS-024629)
- Shichao Chen
- Yun-peng Zhao
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2019, Dong et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Natural selection and repeated patterns of molecular evolution following allopatric divergence
eLife 8:e45199.
https://doi.org/10.7554/eLife.45199
Further reading
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- Evolutionary Biology
The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than 10 alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognised.
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- Computational and Systems Biology
- Evolutionary Biology
As pathogens spread in a population of hosts, immunity is built up, and the pool of susceptible individuals are depleted. This generates selective pressure, to which many human RNA viruses, such as influenza virus or SARS-CoV-2, respond with rapid antigenic evolution and frequent emergence of immune evasive variants. However, the host’s immune systems adapt, and older immune responses wane, such that escape variants only enjoy a growth advantage for a limited time. If variant growth dynamics and reshaping of host-immunity operate on comparable time scales, viral adaptation is determined by eco-evolutionary interactions that are not captured by models of rapid evolution in a fixed environment. Here, we use a Susceptible/Infected model to describe the interaction between an evolving viral population in a dynamic but immunologically diverse host population. We show that depending on strain cross-immunity, heterogeneity of the host population, and durability of immune responses, escape variants initially grow exponentially, but lose their growth advantage before reaching high frequencies. Their subsequent dynamics follows an anomalous random walk determined by future escape variants and results in variant trajectories that are unpredictable. This model can explain the apparent contradiction between the clearly adaptive nature of antigenic evolution and the quasi-neutral dynamics of high-frequency variants observed for influenza viruses.
